Laminar interactions in rat motor cortex during cyclical excitability changes of the penicillin focus.

Laminar interactions between neurons in rat motor cortex during cyclical seizure episodes in the penicillin focus were studied using a combination of current source-density (CSD) and principal component analysis (PCA), combined with computer-based physical modeling. These data suggest that all phases of cyclical seizure phenomena are produced by interactions between two distinct populations of neurons, the same neuronal circuits previously reported to give rise to the direct cortical response (DCR) and electrically evoked interictal penicillin spikes (EIIS). The first population consists of small pyramidal cells in the supragranular layer, and the second population consists of larger pyramidal cells in the infragranular layers with apical dendrites extending to the cortical surface. The supragranular cells serve as a trigger zone for initiating both spontaneous interictal spikes (IIS) and polyspike bursts (PSB) during seizures. Fast activity in the supragranular cells is typically followed by a hyperpolarizing slow wave that may be the result of Ca2+-activated K+ currents. This slow wave increases during seizures, possibly reflecting changes in extracellular Ca2+ associated with seizure onset and termination. The monophasic response of infragranular cells is similar for both IIS and PSB and consists of a large depolarizing shift followed by a rapid but partial repolarization period and a subsequent gradual repolarization period lasting several hundred milliseconds. The infragranular response is similar in polarity and morphology to the intracellularly recorded paroxysmal depolarization shift (PDS) and may indicate that these deeper neurons are mainly responsible for this phenomena in neocortex. Finally, there is a marked postictal slow oscillation between the supra- and infragranular layers. This oscillation appears first and largest in the supragranular cells and may reflect a disturbance in excitatory feedback in these cells produced by the disinhibitory effect of penicillin, a disturbance capable of pathologically synchronizing the epileptic neuronal aggregate sufficiently for activation of the spike-generating mechanism and subsequent seizures.